• 1

    Petney TN, Andrews RH, 1998. Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. Int J Parasitol 28 :377–393.

    • Search Google Scholar
    • Export Citation
  • 2

    Drake LJ, Bundy DAP, 2001. Multiple helminth infections in children: impact and control. Parasitology 122 (Suppl.):S73–S81.

  • 3

    Stoll NR, 1947. This wormy world. J Parasitol 33 :1–18.

  • 4

    Buck AA, Anderson RI, MacRae AA, 1978. Epidemiology of poly-parasitism. I. Occurrence, frequency and distribution of multiple infections in rural communities in Chad, Peru, Afghanistan, and Zaire. Tropenmed Parasitol 29 :61–70.

    • Search Google Scholar
    • Export Citation
  • 5

    Cox FEG, 2001. Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl):S23–S38.

  • 6

    Keiser J, N’Goran EK, Traoré M, Lohourignon KL, Singer BH, Lengeler C, Tanner M, Utzinger J, 2002. Polyparasitism with Schistosoma mansoni, geohelminths, and intestinal protozoa in rural Côte d’Ivoire. J Parasitol 88 :461–466.

    • Search Google Scholar
    • Export Citation
  • 7

    de Silva NR, 2003. Impact of mass chemotherapy on the morbidity due to soil-transmitted nematodes. Acta Trop 86 :197–214.

  • 8

    Ezeamama AE, Friedman JF, Olveda RM, Acosta LP, Kurtis JD, Mor V, McGarvey ST, 2005. Functional significance of low-intensity polyparasite helminth infections in anemia. J Infect Dis 192 :2160–2170.

    • Search Google Scholar
    • Export Citation
  • 9

    Raso G, Luginbühl A, Adjoua CA, Tian-Bi NT, Silué KD, Matthys B, Vounatsou P, Wang YL, Dumas ME, Holmes E, Singer BH, Tanner M, N’Goran EK, Utzinger J, 2004. Multiple parasite infections and their relationship to self-reported morbidity in a community of rural Côte d’Ivoire. Int J Epidemiol 33 :1092–1102.

    • Search Google Scholar
    • Export Citation
  • 10

    Howard SC, Donnell CA, Chan MS, 2001. Methods for estimation of associations between multiple species parasite infections. Parasitology 122 :233–251.

    • Search Google Scholar
    • Export Citation
  • 11

    Waikagul J, Krudsood S, Radomyos P, Radomyos B, Chalemrut K, Jonsuksuntigul P, Kojima S, Looareesuwan S, Thaineau W, 2002. A cross-sectional study of intestinal parasitic infections among schoolchildren in Nan province, northern Thailand. Southeast Asian J Trop Med Public Health 33 :218–223.

    • Search Google Scholar
    • Export Citation
  • 12

    Nielsen PB, Mojon M, 1987. Improved diagnosis of Strongyloides stercoralis by seven consecutive stool specimens. Zentralbl Bakteriol Mikrobiol Hyg A 263 :616–618.

    • Search Google Scholar
    • Export Citation
  • 13

    de Vlas SJ, Gryseels B, 1992. Underestimation of Schistosoma mansoni prevalences. Parasitol Today 8 :274–277.

  • 14

    Marti H, Koella JC, 1993. Multiple stool examinations for ova and parasites and rate of false-negative results. J Clin Microbiol 31 :3044–3045.

    • Search Google Scholar
    • Export Citation
  • 15

    Booth M, Vounatsou P, N’Goran EK, Tanner M, Utzinger J, 2003. The influence of sampling effort and the performance of the Kato–Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Côte d’Ivoire. Parasitology 127 :525–531.

    • Search Google Scholar
    • Export Citation
  • 16

    van Gool T, Weijts R, Lommerse E, Mank TG, 2003. Triple faeces test: an effective tool for detection of intestinal parasites in routine clinical practice. Eur J Clin Microbiol Infect Dis 22 :284–290.

    • Search Google Scholar
    • Export Citation
  • 17

    Brooker S, Miguel EA, Moulin S, Luoba AI, Bundy DAP, Kremer M, 2000. Epidemiology of single and multiple species of helminth infections among school children in Busia district, Kenya. East Afr Med J 77 :157–161.

    • Search Google Scholar
    • Export Citation
  • 18

    Thiongo FW, Luoba A, Ouma JH, 2001. Intestinal helminths and schistosomiasis among school children in a rural district in Kenya. East Afr Med J 78 :279–282.

    • Search Google Scholar
    • Export Citation
  • 19

    Tchuem Tchuenté LA, Behnke JM, Gilbert FS, Southgate VR, Vercruysse J, 2003. Polyparasitism with Schistosoma haematobium and soil-transmitted helminth infections among school children in Loum, Cameroon. Trop Med Int Health 8 :975–986.

    • Search Google Scholar
    • Export Citation
  • 20

    Giboda M, Viengsay M, Bouaphan S, Ditrich O, 1991. Épidémiologie des parasitoses intestinales au Laos. Bull Soc Pathol Exot 84 :184–193.

    • Search Google Scholar
    • Export Citation
  • 21

    Booth M, Guyatt HL, Li YS, Tanner M, 1996. The morbidity attributable to Schistosoma japonicum infection in 3 villages in Dongting Lake region, Hunan province, PR China. Trop Med Int Health 1 :646–654.

    • Search Google Scholar
    • Export Citation
  • 22

    Needham C, Kim HT, Hoa NV, Cong LD, Michael E, Drake L, Hall A, Bundy DAP, 1998. Epidemiology of soil-transmitted nematode infections in Ha Nam province, Vietnam. Trop Med Int Health 3 :904–912.

    • Search Google Scholar
    • Export Citation
  • 23

    Yu SH, Xu LQ, Jiang ZX, Xu SH, Han JJ, Zhu YG, Chang J, Lin JX, Xu FN, 1994. Nationwide survey of human parasite in China. Southeast Asian J Trop Med Public Health 25 :4–10.

    • Search Google Scholar
    • Export Citation
  • 24

    Chinese Ministry of Health, 2005. Report on the national survey of current situation of major human parasitic diseases in China. Shanghai: National Institute of Parasitic Diseases, China CDC, 1–33.

  • 25

    Li LH, Zhou XN, Du ZW, Wang XZ, Wang LB, Jiang JY, Yoshikawa H, Steinmann P, Utzinger J, Wu Z, Chen JX, Chen SH, Zhang L, 2007. Molecular epidemiology of human Blastocystis in a village in Yunnan province, China. Parasitol Int 56 :281–286.

    • Search Google Scholar
    • Export Citation
  • 26

    Steinmann P, Zhou XN, Du ZW, Jiang JY, Wang LB, Wang XZ, Li LH, Marti H, Utzinger J, 2007. Occurrence of Strongyloides stercoralis in Yunnan province, China, and comparison of diagnostic methods. PLoS Negl Trop Dis 1 :e75.

    • Search Google Scholar
    • Export Citation
  • 27

    Katz N, Chaves A, Pellegrino J, 1972. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14 :397–400.

    • Search Google Scholar
    • Export Citation
  • 28

    García LS, 2007. Diagnostic medical parasitology. Washington, D.C.: ASM Press, 1–1202.

  • 29

    Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Ieda M, Takatsuka N, Kita K, Ohtomo H, 1991. A modified agar plate method for detection of Strongyloides stercoralis. Am J Trop Med Hyg 45 :518–521.

    • Search Google Scholar
    • Export Citation
  • 30

    Kitvatanachai S, Pipitgool V, 1999. Efficacy of three methods in the detection of hookworm and Strongyloides stercoralis infections. J Trop Med Parasitol 22 :80–81.

    • Search Google Scholar
    • Export Citation
  • 31

    Marti H, Escher E, 1990. SAF—an alternative fixation solution for parasitological stool specimens. Schweiz Med Wochenschr 120 :1473–1476.

    • Search Google Scholar
    • Export Citation
  • 32

    WHO, 2002. Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee. WHO Tech Rep Ser 912 :1–57.

    • Search Google Scholar
    • Export Citation
  • 33

    Bogoch I, Raso G, N’Goran EK, Marti HP, Utzinger J, 2006. Differences in microscopic diagnosis of helminths and intestinal protozoa among diagnostic centres. Eur J Clin Microbiol Infect Dis 25 :344–347.

    • Search Google Scholar
    • Export Citation
  • 34

    Montresor A, Zin TT, Padmasiri E, Allen H, Savioli L, 2004. Soil-transmitted helminthiasis in Myanmar and approximate costs for countrywide control. Trop Med Int Health 9 :1012–1015.

    • Search Google Scholar
    • Export Citation
  • 35

    Rim HJ, Chai JY, Min DY, Cho SY, Eom KS, Hong SJ, Sohn WM, Yong TS, Deodato G, Standgaard H, Phommasack B, Yun CH, Hoang EH, 2003. Prevalence of intestinal parasite infections on a national scale among primary schoolchildren in Laos. Parasitol Res 91 :267–272.

    • Search Google Scholar
    • Export Citation
  • 36

    Steinmann P, Zhou XN, Li YL, Li HJ, Chen SR, Yang Z, Fan W, Jia TW, Li LH, Vounatsou P, Utzinger J, 2007. Helminth infections and risk factor analysis among residents in Eryuan county, Yunnan province, China. Acta Trop 104 :38–51.

    • Search Google Scholar
    • Export Citation
  • 37

    Utzinger J, Booth M, N’Goran EK, Müller I, Tanner M, Lengeler C, 2001. Relative contribution of day-to-day and intra-specimen variation in faecal egg counts of Schistosoma mansoni before and after treatment with praziquantel. Parasitology 122 :537–544.

    • Search Google Scholar
    • Export Citation
  • 38

    Engels D, Sinzinkayo E, Gryseels B, 1996. Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implications. Am J Trop Med Hyg 54 :319–324.

    • Search Google Scholar
    • Export Citation
  • 39

    Yu JM, de Vlas SJ, Yuan HC, Gryseels B, 1998. Variations in fecal Schistosoma japonicum egg counts. Am J Trop Med Hyg 59 :370–375.

  • 40

    Martin LK, Beaver PC, 1968. Evaluation of Kato thick-smear technique for quantitative diagnosis of helminth infections. Am J Trop Med Hyg 17 :382–391.

    • Search Google Scholar
    • Export Citation
  • 41

    Dacombe RJ, Crampin AC, Floyd S, Randall A, Ndhlovu R, Bickle Q, Fine PEM, 2007. Time delays between patient and laboratory selectively affect accuracy of helminth diagnosis. Trans R Soc Trop Med Hyg 101 :140–145.

    • Search Google Scholar
    • Export Citation
  • 42

    Utzinger J, N’Goran EK, N’Dri A, Lengeler C, Tanner M, 2000. Efficacy of praziquantel against Schistosoma mansoni with particular consideration for intensity of infection. Trop Med Int Health 5 :771–778.

    • Search Google Scholar
    • Export Citation
  • 43

    Utzinger J, Vounatsou P, N’Goran EK, Tanner M, Booth M, 2002. Reduction in the prevalence and intensity of hookworm infections after praziquantel treatment for schistosomiasis infection. Int J Parasitol 32 :759–765.

    • Search Google Scholar
    • Export Citation
  • 44

    Fenwick A, 2006. New initiatives against Africa’s worms. Trans R Soc Trop Med Hyg 100 :200–207.

  • 45

    Brooker S, Clements ACA, Bundy DAP, 2006. Global epidemiology, ecology and control of soil-transmitted helminth infections. Adv Parasitol 62 :221–261.

    • Search Google Scholar
    • Export Citation
  • 46

    Utzinger J, de Savigny D, 2006. Control of neglected tropical diseases: integrated chemotherapy and beyond. PLoS Med 3 :e112.

  • 47

    de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L, 2003. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol 19 :547–551.

    • Search Google Scholar
    • Export Citation
  • 48

    Cringoli G, 2004. La diagnostica coprologica: quali novità. Parassitologia 46 :137–139.

  • 49

    Cringoli G, 2006. FLOTAC, a novel apparatus for a multivalent faecal egg count technique. Parassitologia 48 :381–384.

  • 50

    Utzinger J, Rinaldi L, Lohourignon LK, Rohner F, Zimmermann MB, Tschannen AB, N’Goran EK, Cringoli G, 2008. FLO-TAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Trans R Soc Trop Med Hyg 102 :84–90.

    • Search Google Scholar
    • Export Citation
  • 51

    Utzinger J, Keiser J, 2004. Schistosomiasis and soil-transmitted helminthiasis: common drugs for treatment and control. Expert Opin Pharmacother 5 :263–285.

    • Search Google Scholar
    • Export Citation
  • 52

    Farthing MJ, 2006. Treatment options for the eradication of intestinal protozoa. Nat Clin Pract Gastroenterol Hepatol 3 :436–445.

  • 53

    WHO, 2006. Preventive chemotherapy in human helminthiasis: coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers. Geneva: World Health Organization, 1–62.

  • 54

    Olsen A, 2007. Efficacy and safety of drug combinations in the treatment of schistosomiasis, soil-transmitted helminthiasis, lymphatic filariasis and onchocerciasis. Trans R Soc Trop Med Hyg 101 :747–758.

    • Search Google Scholar
    • Export Citation
  • 55

    García HH, Gonzalez AE, Evans CA, Gilman RH, 2003. Taenia solium cysticercosis. Lancet 362 :547–556.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Extensive Multiparasitism in a Village of Yunnan Province, People’s Republic of China, Revealed by a Suite of Diagnostic Methods

View More View Less
  • 1 Department of Public Health and Epidemiology, Swiss Tropical Institute, Basel, Switzerland; Helminthiasis Division, Yunnan Institute of Parasitic Diseases, Simao, People’s Republic of China; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People’s Republic of China; Department of Medical and Diagnostic Services, Swiss Tropical Institute, Basel, Switzerland

Intestinal multiparasitism, the accuracy of different diagnostic techniques, and the influence of sampling effort were studied among 215 individuals in a Bulang village, Yunnan province, People’s Republic of China. Behavioral, demographic, and socioeconomic data were obtained by questionnaire. Multiple stool specimens were examined by the Kato–Katz, Koga agar plate, Baermann, and ether–concentration methods. Eight helminth and 7 protozoa species were diagnosed. The prevalence of each of the 3 main soil-transmitted helminths (Ascaris lumbricoides, hookworm, and Trichuris trichiura) exceeded 85%. Blastocystis hominis was the most prevalent intestinal protozoan (20.0%). Over 80% of the individuals harbored 3 or more intestinal parasites concurrently. The infection intensities were predominantly light for hookworm and T. trichiura but moderate for A. lumbricoides. Examination of 3 instead of 1 stool specimen increased the sensitivity of helminth diagnosis, most notably for hookworm. Intestinal multiparasitism is rampant in this rural part of Yunnan province and calls for control measures.

Author Notes

Reprint requests: Jürg Utzinger, Department of Public Health and Epidemiology, Swiss Tropical Institute, P.O. Box, CH-4002 Basel, Switzerland, Tel: 41-61-284-8129, Fax: 41-61-284-8105, E-mail: juerg.utzinger@unibas.ch.
Save